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Eco-Evolutionary Dynamics of Sexual Dimorphism

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Eco-Evolutionary Dynamics of Sexual Dimorphism TREE 2534 No. of Pages 4 Forum Eco-Evolutionary sexual dimorphism (i.e., the trait differences Studies that correlate variation in ecologi- between females and males; arrow 2 in cal conditions to population or species Dynamics of Sexual Figure 1B). Sexual dimorphism is ubiquitous variation in dimorphism are informative Dimorphism in nature and encompasses a varietyoftraits but cannot distinguish ecological causes that may impact communityandecosystem from effects of dimorphism (e.g., [7]). 1,2, ,@ David C. Fryxell , * dynamics. Given the recent interest in Thus, experimental manipulations are 2,@ Doriane E. Weiler, understanding community and ecosystem needed to test for community and eco- 3,@ effects of intraspecific trait variation in gen- system effects of sexual dimorphism. Michael T. Kinnison, and 2,@ eral [4], the lack of empirical research on the Such direct tests have only recently Eric P. Palkovacs ecological consequences of sexual dimor- emerged (arrow 3, Figure 1B) and have phism is surprising (arrow 3, Figure 1B). been performed at two levels of biological Sexual dimorphism is widespread, organization: the individual level and the but we have a limited understand- Evolved Sexual Dimorphism in population level. ing of its significance for commu- Ecological Roles nities and ecosystems. Several There has long been evidence of ecologi- The Extended Phenotype of new experiments demonstrate that cal dimorphism (i.e., sexual dimorphism in Dimorphism sexual dimorphism can have far- ecological roles). For example, the sexes Sex differences at the individual level can reaching ecological effects. These commonly differ in diets in the field. These have community and ecosystem conse- results suggest that sexual dimor- effects may be pronounced in cases of quences when communities assemble or ‘ phism and sexual selection are sexual size dimorphism, in which the ecosystems exist as extended pheno- ’ potent, but largely overlooked larger sex can feed on larger prey. In types of individual hosts (i.e., foundation species without strong size dimorphism, species). For example, Nell and col- components of eco-evolutionary dynamics. ecological dimorphism may still be strong leagues [8] demonstrated that female due to dimorphism in functional traits. For genotypes of the mulefat shrub (Baccha- example, the sexes of the recently extinct ris salicifolia) had more flowers and grew Eco-evolutionary dynamics describe huia (Heteralocha acutirostris), a New more quickly than did male genotypes reciprocal effects between evolution and Zealand bird species that exhibited one cultivated in the same garden population, community, and ecosystem of the most extreme cases of sexual (Figure 2C). This trait dimorphism led to ecology. These dynamics can be broadly dimorphism in beak shape known, must dimorphism in hosted arthropod commu- important when natural selection causes have fed on significantly different resour- nity composition; the more flower-laden rapid trait changes to occur in a population, ces (Figure 2A) [5]. Another extreme eco- females had higher predator densities, because the trait changes can have com- logical dimorphism is found in adult presumably because of increased visita- munity- and ecosystem-wide consequen- mosquitoes: females feed on animal tion by nectar-feeding insect prey. Simi- ces [1] (Figure 1A). There may also be blood, while males feed on plant nectar larly, Tsuji and Fukami [9] studied the ecological consequences of evolutionary (e.g., Ochlerotatus sp., Figure 2B). microbe communities assembling on responses to sexual selection. This male versus female flowers in the dioe- hypothesis is primarily supported by theory Ecological dimorphism could be significant cious shrub Eurya emarginata (Figure 2D). and experiments demonstrating that sex- even when sexual dimorphism is relatively Female flowers contained less nectar and ual selection can affect population ecology inconspicuous. Forexample, thesexes may had significantly lower bacterial and fun- [2] and by work showing that sexual selec- show little morphological dimorphism, but gal concentrations compared with male tion can affect functional traits (i.e., those ecological dimorphism could arise from dif- flowers, apparently a result of differential hypothesized to have community or eco- ferential habitat use [6]. More generally, it visitation by insects. Based on this and system effects) [3]. However, the role of may be that most sexual organisms display related work, it may be that microbiomes sexual selection in communities and eco- some degree of ecological dimorphism due are commonly forms of ‘extended sexual systems remains largely untested. to divergent nutritional requirements dimorphism’ in plants and animals. between the sexes, a product of differential Selection has community and ecosystem reproductive investment. Even weak dimor- Studyingsexualdimorphismintheextended consequences through its effects on traits phism could be important for communities phenotypes of foundation species provides (Figure 1). Sexual selection can shape the and ecosystems in abundant or otherwise a clear-cut relationship between sexual trait distribution of a population by affecting ecologically important populations. dimorphism and community and Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy 1 TREE 2534 No. of Pages 4 (A) (B) Natura l Natural Sexual sele con selecon selecon Evoluon 1 2 Feedback Popu laon Nondimorphic Sexua l fun conal trait 5 4 traits dimorph ism distrib uon E.g., species interacons 3 Community and Commun ity and ecosystem ecosyst em ecology ecolo gy Figure 1. The Conceptual Model. (A) The field of ‘eco-evolutionary dynamics’ has classically focused on the community and ecosystem effects of evolution by natural selection (blue arrows) and has not focused on sexually dimorphic traits. The field has further aimed to parse feedbacks between evolution and ecology when they act on similar timescales. (B) Recently, researchers have called for the explicit incorporation of sexual selection into this framework [2,3], which we expand in our conceptual model to include two separate aspects of the trait distribution of a population: sexually dimorphic traits and nondimorphic traits. While both natural selection (1) and sexual selection (2) affect sexual dimorphism (together, an effect referred to as ‘sex-specific selection’), to understand the link between sexual selection and communities and ecosystems, we must understand the effect of sexual dimorphism on communities and ecosystems (3). Given that communities and ecosystems shape sexual selection (4) and natural selection (5), future work could aim to parse eco-evolutionary feedbacks associated with sexual dimorphism. ecosystem ecology. However, there is often seeks to compare differences in effects of ecological effects of mosquitofish are interest in communities and ecosystems populations with trait distributions that are largely shaped by the sex ratio of popula- assembling at larger spatial scales than more female or male biased. tions, which vary widely in nature. those associated with individual hosts. Moreover, from the eco-evolutionary Fryxell and colleagues [10] manipulated In the other sex ratio experiment, Start dynamics perspective, the overarching goal population sex ratios of sexually dimorphic and De Lisle [11] manipulated sex ratios is to test the ecological effects of evolution- mosquitofish (Gambusia affinis) in pond of predaceous newts (Notophthalmus vir- ary change, which occurs in populations. mesocosms(Figure2E).Incontrasttomale idescens) in pond mesocosms Thus, the unifying level of analysis for under- mosquitofish, females exhibit continuous (Figure 2F). While these newts do not standing the effects of sexual dimorphism growth and have higher feeding and excre- show strong differences in feeding traits on communities and ecosystems, and tion rates. In pond mesocosms, female- per se, the sexes differ substantially in incorporating those effects into an eco-evo- biased populations induced stronger tro- habitat use. Results showed that lutionary perspective, is at the population phic cascades, causing changes even to female-biased populations spent more level. ecosystem properties such as water tem- time in the benthic zone and grazed down perature and pH. When comparing the benthic prey relative to pelagic prey, thus Populations Link Dimorphism Evo effect size of sex ratio (female-biased vs. inducing a community shift towards the to Eco male-biased) to the effect size of mosquito- dominance of pelagic prey. These results To date, effects of sexual dimorphism fish presence versus absence, sex ratio highlight that, even in cases of inconspic- have been studied experimentally at the effects were up to approximately half as uous morphological dimorphism, ecologi- population level through the manipulation strong as the effects of mosquitofish pres- cal effects of sexual dimorphism can still of population sex ratios. This approach ence itself. Thus, the strong and diverse be significant. 2 Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy TREE 2534 No. of Pages 4 (A) (B) (C) (D) (E) (F) Figure 2. Taxa Described in the Main Text. Some of these taxa have hypothesized community and ecosystem effects of sexual dimorphism, (A) huia (Heteralocha acutirostris) and (B) mosquitoes (e.g., Ochlerotatus sp., pictured), whereas others from recent experiments show significant effects of sexual dimorphism, (C) mulefat (Baccharis salicifolia), a dioecious shrub from the American southwest; (D) a dioecious shrub
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